Early offspring separation from mothers causes social deprivation. Mouthbrooding, when eggs and fry are incubated in the buccal cavity of the parent, is one of the reproductive strategies in fish. The mother is the incubating parent in African lake cichlids from the genus Tropheus. Many of these are produced in captivity and some producers use artificial incubators in which eggs are incubated separately from the mother. We hypothesized that this practice may dramatically modify the reproduction rate of fish individuals produced by the method of artificial incubation. The long-term experiment focused on Tropheus sp. "Caramba" had been carried out for 10 years when maternally incubated and separated individuals were compared. We found a negative effect of artificial egg and offspring incubation out of the mother's buccal cavity. The deprived females laid the same number of eggs as maternally incubated females, but most eggs were lost during the incubation. Moreover, the reproduction frequency was significantly lower in deprived females in comparison with those maternally incubated. This study should be perceived as preliminary. For this reason and with respect to welfare principles, we strongly recommend similarly designed experiments focused on other potentially sensitive fish mouthbrooders. Once the syndrome would be confirmed, we recommend avoiding artificial incubation of mouthbrooding fish in general.

1st Faculty of Medicine Charles University Kateřinská 32 12108 Prague Czech Republic

Department of Physiology Faculty of Science Charles University Viničná 7 12844 Prague Czech Republic

Department of Zoology and Fisheries Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague Kamýcká 129 16500 Prague Suchdol Czech Republic

Department of Zoology Faculty of Science Charles University Viničná 7 12844 Prague Czech Republic

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Latham NR, Mason GJ. Maternal deprivation and the development of stereotypic behaviour. Appl. Anim. Behav. Sci. 2008;110:84–108. doi: 10.1016/j.applanim.2007.03.026. DOI

Patoka J, Kalous L, Bartoš L. Early ontogeny social deprivation modifies future agonistic behaviour in crayfish. Sci. Rep. 2019;9:4667. doi: 10.1038/s41598-019-41333-8. PubMed DOI PMC

Gruendel AD, Arnold WJ. Effects of early social deprivation on reproductive behavior of male rats. J. Comp. Physiol. Psych. 1969;67:123–128. doi: 10.1037/h0026667. PubMed DOI

Harlow HF, Harlow M. Social deprivation in monkeys. Sci. Am. 1962;207:136–146. doi: 10.1038/scientificamerican1162-136. PubMed DOI

Zeytinoglu, S. & Fox, N. A. in The Handbook of Solitude: Psychological Perspectives on Social Isolation, Social Withdrawal, and Being Alone (eds Robert J Coplan, Julie C Bowker, & Larry J Nelson) Ch. 4, 42–57 (John Wiley & Sons, 2021).

Bertin A, Richard-Yris MA. Mothering during early development influences subsequent emotional and social behaviour in Japanese quail. J. Exp. Zool. Part A. 2005;303:792–801. doi: 10.1002/jez.a.202. PubMed DOI

Tóth M, Halász J, Mikics É, Barsy B, Haller J. Early social deprivation induces disturbed social communication and violent aggression in adulthood. Behav. Neurosci. 2008;122:849–854. doi: 10.1037/0735-7044.122.4.849. PubMed DOI

Antunes DF, et al. Early social deprivation shapes neuronal programming of the social decision-making network in a cooperatively breeding fish. Mol. Ecol. 2021;30:4118–4132. doi: 10.1111/mec.16019. PubMed DOI PMC

Chen P, Hong W. Neural circuit mechanisms of social behavior. Neuron. 2018;98:16–30. doi: 10.1016/j.neuron.2018.02.026. PubMed DOI PMC

Anderson DJ, Perona P. Toward a science of computational ethology. Neuron. 2014;84:18–31. doi: 10.1016/j.neuron.2014.09.005. PubMed DOI

Groneberg, A. H. et al. Early-life social experience shapes social avoidance reactions in larval zebrafish. Curr. Biol.30, 4009–4021. e4004. 10.1016/j.cub.2020.07.088 (2020). PubMed

Novák, J. et al. Ornamental aquaculture significantly affected by the “Czech aquarium phenomenon”. Aquaculture555, 738259. 10.1016/j.aquaculture.2022.738259 (2022).

Maceda-Veiga A, Domínguez-Domínguez O, Escribano-Alacid J, Lyons J. The aquarium hobby: Can sinners become saints in freshwater fish conservation? Fish. Fish. 2016;17:860–874. doi: 10.1111/faf.12097. DOI

Evers HG, Pinnegar JK, Taylor MI. Where are they all from?—sources and sustainability in the ornamental freshwater fish trade. J. Fish Biol. 2019 doi: 10.1111/jfb.13930. PubMed DOI

Novák J, Kalous L, Patoka J. Modern ornamental aquaculture in Europe: Early history of freshwater fish imports. Rev. Aquacult. 2020;12:2042–2060. doi: 10.1111/raq.12421. DOI

Tapkir, S. D. et al. Far from home: Tracking the global ornamental fish trade in endangered zebra loach, Botia striata, from freshwater ecoregion and biodiversity hotspot in India. J. Nat. Conserv.61, 126007. 10.1016/j.jnc.2021.126007 (2021).

Sefc, K. M. Mating and parental care in Lake Tanganyika's cichlids. Int. J. Evol. Biol.2011, 470875. 10.4061/2011/470875 (2011). PubMed PMC

Taborsky B, Foerster K. Female mouthbrooders adjust incubation duration to perceived risk of predation. Anim. Behav. 2004;68:1275–1281. doi: 10.1016/j.anbehav.2004.03.005. DOI

Abecia JR, et al. Diverse parentage relationships in paternal mouthbrooding fishes. Biol. Lett. 2022;18:20210576. doi: 10.1098/rsbl.2021.0576. PubMed DOI PMC

Balon EK. Reproductive guilds of fishes: A proposal and definition. J. Fish. Res. Board Can. 1975;32:821–864. doi: 10.1139/f75-110. DOI

Butler, J. M. & Maruska, K. P. Noise during mouthbrooding impairs maternal care behaviors and juvenile development and alters brain transcriptomes in the African cichlid fish Astatotilapia burtoni. Genes Brain Behav.20, e12692. 10.1111/gbb.12692 (2021). PubMed

Watanabe WO, Smith SJ, Wicklund RI, Olla BL. Hatchery production of Florida red tilapia seed in brackishwater tanks under natural-mouthbrooding and clutch-removal methods. Aquaculture. 1992;102:77–88. doi: 10.1016/0044-8486(92)90290-2. DOI

Oliveros, S. L., Hernández Paniagua, K. J., Pimentel-Parra, G. A., Murcia-Ordonez, B. & Chaves-Moreno, L. C. Evaluation of the efficiency of three incubator models with different flows in larval development of Osteoglossum bicirrhosum (silver arowana). Rev. de Investig. Vet. del Peru29, 514–521. 10.15381/rivep.v29i2.12681 (2018).

Santos ME, Lopes JF, Kratochwil CF. East African cichlid fishes. EvoDevo. 2023;14:1–21. doi: 10.1186/s13227-022-00205-5. PubMed DOI PMC

Brooks GB., Jr A simple self-contained incubator for cichlid eggs. N. Am. J. Aquacult. 2002;64:164–166. doi: 10.1577/1548-8454(2002)064<0164:ASSCIF>2.0.CO;2. DOI

Kanitz E, Tuchscherer M, Puppe B, Tuchscherer A, Stabenow B. Consequences of repeated early isolation in domestic piglets (Sus scrofa) on their behavioural, neuroendocrine, and immunological responses. Brain. Behav. Immun. 2004;18:35–45. doi: 10.1016/S0889-1591(03)00085-0. PubMed DOI

Jonsson B, Jonsson N. Early environment influences later performance in fishes. J. Fish Biol. 2014;85:151–188. doi: 10.1111/jfb.12432. PubMed DOI

Gómez-Laplaza LM, Gil-Carnicero P. Imprinting in fish: A Little explored phenomenon with possible implications for fish welfare. Annu. Rev. Biomed. Sci. 2008;10:51–62. doi: 10.5016/1806-8774.2008.v10pt51. DOI

Russock HI. filial social bong formation in fry of the maternal mouthbrooding tilapia (Pisces: Cichlidae): A comparative study. Behaviour. 1999;136:567–594. doi: 10.1163/156853999501478. DOI

Sturmbauer C, Koblmüller S, Sefc KM, Duftner N. Phylogeographic history of the genus Tropheus, a lineage of rock-dwelling cichlid fishes endemic to Lake Tanganyika. Hydrobiologia. 2005;542:335–366. doi: 10.1007/s10750-004-4664-y. DOI

Baric S, Salzburger W, Sturmbauer C. Phylogeography and evolution of the Tanganyikan cichlid genus Tropheus based upon mitochondrial DNA sequences. J. Mol. Evol. 2003;56:54–68. doi: 10.1007/s00239-002-2380-7. PubMed DOI

Kimball ME, Miller JM, Whitfield PE, Hare JA. Thermal tolerance and potential distribution of invasive lionfish(Pterois volitans/miles complex) on the east coast of the United States. Mar. Ecol. Prog. Ser. 2004;283:269–278. doi: 10.3354/meps283269. DOI

Wickler W. Zur Soziologie des Brabantbuntbarsches, Tropheus moorei (Pisces, Cichlidae) Z. Tierpsychol. 1969;26:967–987. doi: 10.1111/j.1439-0310.1969.tb01985.x. DOI

Palagi E, Barbuti R, Norscia I. Aquarium cichlid fish Tropheus moorii flexibly adjust hierarchy when tank fish species composition changes: A pilot study. J. Zoo Aquar. Res. 2020;8:86–93. doi: 10.19227/jzar.v8i2.381. DOI

Schneidewind, F. Das große Buch der Tropheus-Cichliden. 103 (bede-Verlag, 1996).

Maestripieri D. Maternal influences on primate social development. Behav. Ecol. Sociobiol. 2018;72:130. doi: 10.1007/s00265-018-2547-x. DOI

Soares MC, Oliveira RF, Ros AF, Grutter AS, Bshary R. Tactile stimulation lowers stress in fish. Nat. Commun. 2011;2:534. doi: 10.1038/ncomms1547. PubMed DOI

Crapon de Caprona, M.-D. The influence of early experience on preferences for optical and chemical cues produced by both sexes in the cichlid fish Haplochromis burtoni (Astatotilapia burtoni, Greenwood 1979). Zeitschrift für Tierpsychologie. 10.1111/j.1439-0310.1982.tb00325.x (1982).

Patil SSS, Nayak MS. Gonadal maturation, courtship behavior and parental care in Oreochromis mossambicus. Int. J. Innov. Res. Adv. Stud. 2016;3:126–130.

Barlow GW. Guest commentary: How to observe and report mouthbrooding in cichlid fishes. Cichlid News. 2000;6:24–31.

Novák J. Cichlidy rodu Tropheus. Akvárium terárium. 1993;36:2–5.

McLennan DA. A phylogenetic approach to the evolution of fish behaviour. Rev. Fish. Biol. Fisher. 1994;4:430–460. doi: 10.1007/BF00042889. DOI

Nelson, J. S., Grande, T. C. & Wilson, M. V. Fishes of the World. (John Wiley & Sons, 2016).

Sterba, G. Süsswasserfische der Welt. (Urania - Verlag, 1987).

Blažek, R. et al. Success of cuckoo catfish brood parasitism reflects coevolutionary history and individual experience of their cichlid hosts. Sci. Adv.4, eaar4380. 10.1126/sciadv.aar4380 (2018). PubMed PMC

Fletcher DE, Dakin EE, Porter BA, Avise JC. Spawning behavior and genetic parentage in the pirate perch (Aphredoderus sayanus), a fish with an enigmatic reproductive morphology. Copeia. 2004;1–10:2004. doi: 10.1643/CE-03-160R. DOI

Mrowka W. Filial cannibalism and reproductive success in the maternal mouthbrooding cichlid fish Pseudocrenilabrus multicolor. Behav. Ecol. Sociobiol. 1987;21:257–265. doi: 10.1007/BF00292507. DOI

Sturmbauer C, Hainz U, Baric S, Verheyen E, Salzburger W. Evolution of the tribe Tropheini from Lake Tanganyika: Synchronized explosive speciation producing multiple evolutionary parallelism. Hydrobiologia. 2003;500:51–64. doi: 10.1007/978-94-007-1084-9_3. DOI

Sturmbauer C, Börger C, Van Steenberge M, Koblmüller S. A separate lowstand lake at the northern edge of Lake Tanganyika? Evidence from phylogeographic patterns in the cichlid genus Tropheus. Hydrobiologia. 2017;791:51–68. doi: 10.1007/s10750-016-2939-8. DOI

Pekár S, Brabec M. Generalized estimating equations: A pragmatic and flexible approach to the marginal GLM modelling of correlated data in the behavioural sciences. Ethology. 2018;124:86–93. doi: 10.1111/eth.12713. DOI

Højsgaard S, Halekoh U, Yan J. The R package geepack for generalized estimating equations. J. Stat. Softw. 2006;15:1–11. doi: 10.18637/jss.v015.i02. DOI